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Ecological and network analyses identify four microbial species with potential significance for the diagnosis/treatment of ulcerative colitis (UC)

BACKGROUND: Ulcerative colitis (UC) is one of the primary types of inflammatory bowel disease (IBD), the occurrence of which has been increasing worldwide. Although IBD is an intensively studied human microbiome-associated disease, research on Chinese populations remains relatively limited, particul...

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Autores principales: Li, Wendy, Sun, Yang, Dai, Lin, Chen, Hongju, Yi, Bin, Niu, Junkun, Wang, Lan, Zhang, Fengrui, Luo, Juan, Wang, Kunhua, Guo, Rui, Li, Lianwei, Zou, Quan, Ma, Zhanshan (Sam), Miao, Yinglei
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8097971/
https://www.ncbi.nlm.nih.gov/pubmed/33947329
http://dx.doi.org/10.1186/s12866-021-02201-6
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author Li, Wendy
Sun, Yang
Dai, Lin
Chen, Hongju
Yi, Bin
Niu, Junkun
Wang, Lan
Zhang, Fengrui
Luo, Juan
Wang, Kunhua
Guo, Rui
Li, Lianwei
Zou, Quan
Ma, Zhanshan (Sam)
Miao, Yinglei
author_facet Li, Wendy
Sun, Yang
Dai, Lin
Chen, Hongju
Yi, Bin
Niu, Junkun
Wang, Lan
Zhang, Fengrui
Luo, Juan
Wang, Kunhua
Guo, Rui
Li, Lianwei
Zou, Quan
Ma, Zhanshan (Sam)
Miao, Yinglei
author_sort Li, Wendy
collection PubMed
description BACKGROUND: Ulcerative colitis (UC) is one of the primary types of inflammatory bowel disease (IBD), the occurrence of which has been increasing worldwide. Although IBD is an intensively studied human microbiome-associated disease, research on Chinese populations remains relatively limited, particularly on the mucosal microbiome. The present study aimed to analyze the changes in the mucosal microbiome associated with UC from the perspectives of medical ecology and complex network analysis. RESULTS: In total, 56 mucosal microbiome samples were collected from 28 Chinese UC patients and their healthy family partners, followed by amplicon sequencing. Based on sequencing data, we analyzed species diversity, shared species, and inter-species interactions at the whole community, main phyla, and core/periphery species levels. We identified four opportunistic “pathogens” (i.e., Clostridium tertium, Odoribacter splanchnicus, Ruminococcus gnavus, and Flavonifractor plautii) with potential significance for the diagnosis and treatment of UC, which were inhibited in healthy individuals, but unrestricted in the UC patients. In addition, we also discovered in this study: (i) The positive-to-negative links (P/N) ratio, which measures the balance of species interactions or inhibition effects in microbiome networks, was significantly higher in UC patients, indicating loss of inhibition against potentially opportunistic “pathogens” associated with dysbiosis. (ii) Previous studies have reported conflicting evidence regarding species diversity and composition between UC patients and healthy controls. Here, significant differences were found at the major phylum and core/periphery scales, but not at the whole community level. Thus, we argue that the paradoxical results found in existing studies are due to the scale effect. CONCLUSIONS: Our results reveal changes in the ecology and network structure of the gut mucosal microbiome that might be associated with UC, and these changes might provide potential therapeutic mechanisms of UC. The four opportunistic pathogens that were identified in the present study deserve further investigation in future studies. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12866-021-02201-6.
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spelling pubmed-80979712021-05-06 Ecological and network analyses identify four microbial species with potential significance for the diagnosis/treatment of ulcerative colitis (UC) Li, Wendy Sun, Yang Dai, Lin Chen, Hongju Yi, Bin Niu, Junkun Wang, Lan Zhang, Fengrui Luo, Juan Wang, Kunhua Guo, Rui Li, Lianwei Zou, Quan Ma, Zhanshan (Sam) Miao, Yinglei BMC Microbiol Research BACKGROUND: Ulcerative colitis (UC) is one of the primary types of inflammatory bowel disease (IBD), the occurrence of which has been increasing worldwide. Although IBD is an intensively studied human microbiome-associated disease, research on Chinese populations remains relatively limited, particularly on the mucosal microbiome. The present study aimed to analyze the changes in the mucosal microbiome associated with UC from the perspectives of medical ecology and complex network analysis. RESULTS: In total, 56 mucosal microbiome samples were collected from 28 Chinese UC patients and their healthy family partners, followed by amplicon sequencing. Based on sequencing data, we analyzed species diversity, shared species, and inter-species interactions at the whole community, main phyla, and core/periphery species levels. We identified four opportunistic “pathogens” (i.e., Clostridium tertium, Odoribacter splanchnicus, Ruminococcus gnavus, and Flavonifractor plautii) with potential significance for the diagnosis and treatment of UC, which were inhibited in healthy individuals, but unrestricted in the UC patients. In addition, we also discovered in this study: (i) The positive-to-negative links (P/N) ratio, which measures the balance of species interactions or inhibition effects in microbiome networks, was significantly higher in UC patients, indicating loss of inhibition against potentially opportunistic “pathogens” associated with dysbiosis. (ii) Previous studies have reported conflicting evidence regarding species diversity and composition between UC patients and healthy controls. Here, significant differences were found at the major phylum and core/periphery scales, but not at the whole community level. Thus, we argue that the paradoxical results found in existing studies are due to the scale effect. CONCLUSIONS: Our results reveal changes in the ecology and network structure of the gut mucosal microbiome that might be associated with UC, and these changes might provide potential therapeutic mechanisms of UC. The four opportunistic pathogens that were identified in the present study deserve further investigation in future studies. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12866-021-02201-6. BioMed Central 2021-05-04 /pmc/articles/PMC8097971/ /pubmed/33947329 http://dx.doi.org/10.1186/s12866-021-02201-6 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Li, Wendy
Sun, Yang
Dai, Lin
Chen, Hongju
Yi, Bin
Niu, Junkun
Wang, Lan
Zhang, Fengrui
Luo, Juan
Wang, Kunhua
Guo, Rui
Li, Lianwei
Zou, Quan
Ma, Zhanshan (Sam)
Miao, Yinglei
Ecological and network analyses identify four microbial species with potential significance for the diagnosis/treatment of ulcerative colitis (UC)
title Ecological and network analyses identify four microbial species with potential significance for the diagnosis/treatment of ulcerative colitis (UC)
title_full Ecological and network analyses identify four microbial species with potential significance for the diagnosis/treatment of ulcerative colitis (UC)
title_fullStr Ecological and network analyses identify four microbial species with potential significance for the diagnosis/treatment of ulcerative colitis (UC)
title_full_unstemmed Ecological and network analyses identify four microbial species with potential significance for the diagnosis/treatment of ulcerative colitis (UC)
title_short Ecological and network analyses identify four microbial species with potential significance for the diagnosis/treatment of ulcerative colitis (UC)
title_sort ecological and network analyses identify four microbial species with potential significance for the diagnosis/treatment of ulcerative colitis (uc)
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8097971/
https://www.ncbi.nlm.nih.gov/pubmed/33947329
http://dx.doi.org/10.1186/s12866-021-02201-6
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